Skip to main content
×
Home
    • Aa
    • Aa

The evolution of parasite manipulation of host behaviour: a theoretical analysis

  • R. Poulin (a1)
Abstract
SUMMARY

Parasite-induced modifications of host behaviour are known from a wide range of host-parasite associations. In many cases, these behavioural changes are thought to be adaptive and. benefit the parasite by increasing its probability of successful transmission. However, in many cases, energy spent on host manipulation will not be available for other functions, such as growth. These trade-offs suggest that in the absence of other constraints, natural selection will optimize, and not maximize, the influence of parasites on host behaviour. This argument is developed and expanded into theoretical considerations of the evolution of host behaviour manipulation by parasites. Among populations of the same parasite species or among closely-related species, the optimal investment into manipulation, or optimal manipulative effort (ME*), of individual parasites is predicted to increase as (1) typical infrapopulation size decreases, (2) prevalence increases, (3) the longevity of the infected host, or of the parasite in its host, decreases, (4) passive transmission rates decrease, and (5) parasite fecundity decreases. This evolutionary analysis indicates that ecological and life history variables may have played an important role in the evolution of manipulation of host behaviour by parasites.

Copyright
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

M. Baudoin (1975). Host castration as a parasitic strategy. Evolution 29, 335–52.

W. M. Bethel & J. C. Holmes (1974). Correlation of development of altered evasive behaviour in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with infectivity to the definitive host. Journal of Parasitology 60, 272–4.

L. A. Curtis (1987). Vertical distribution of an estuarine snail altered by a parasite. Science 235, 1509–11.

R. Dawkins (1990). Parasites, desiderata lists and the paradox of the organism. Parasitology 100 (Suppl.), S63–S73.

A. P. Dobson (1988). The population biology of parasiteinduced changes in host behaviour. Quarterly Review of Biology 63, 139–65.

J. A. Endler (1983). Natural selection on color patterns in poeciliid fishes. Environmental Biology of Fishes 9, 173–90.

M. R. L. Forbes (1993). Parasitism and host reproductive effort. Oikos 67, 444–50.

D. F. Fraser & J. F. Gilliam (1987). Feeding under predation hazard: response of the guppy and Hart's rivulus from sites with contrasting predation hazard. Behavioural Ecology and Sociobiology 21, 203–9.

D. W. Hagen & L. G. Gilbertson (1972). Geographic variation and environmental selection in Gasterosteus aculeatus L. in the Pacific Northwest, America. Evolution 26, 3251.

W. D. Hamilton (1964). The genetical evolution of social behaviour, I & II. Journal of Theoretical Biology 7, 152.

S. Helluy & J. C. Holmes (1990). Serotonin, octopamine, and the clinging behaviour induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Canadian Journal of Zoology 68, 1214–20.

H. Hurd (1990). Physiological and behavioural interactions between parasites and invertebrate hosts. Advances in Parasitology 29, 271318.

H. Hurd & S. Fogo (1991). Changes induced by Hymenolepis diminuta (Cestoda) in the behaviour of the intermediate host Tenebrio molitor (Coleoptera). Canadian Journal of Zoology 69, 2291–4.

K. D. Lafferty (1992). Foraging on prey that are modified by parasites. American Naturalist 140, 854–67.

M. Lloyd (1967). Mean crowding. Journal of Animal Ecology 36, 130.

C. P. Lobue & M. A. Bell (1993). Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the threespine stickleback. American Naturalist 142, 725–35.

G. A. Lozano (1991). Optimal foraging theory: a possible role for parasites. Oikos 60, 391–5.

L. Margolis , G. W. Esch , J. C. Holmes , A. M. Kuris & G. A. Schad (1982). The use of ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131–3.

D. J. Minchella (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–16.

J. Moore (1984). Altered behavioural responses in intermediate hosts: an acanthocephalan parasite strategy. American Naturalist 123, 572–7.

D. F. Oetinger & B. B. Nickol (1982). Spectrophotometric characterization of integumental pigments from uninfected and Acanthocephalus dirus - infected Asellus intermedius. Journal of Parasitology 68, 270–5.

G. O. Poinar Jr. (1991 a). Hairworm (Nematomorpha: Gordioidea) parasites of New Zealand wetas (Orthoptera: Stenopelmatidae). Canadian Journal of Zoology 69, 1592–9.

R. Poulin (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–44.

R. Poulin , M. A. Curtis & M. E. Rau (1992). Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265–71.

T. E. Reimchen (1989). Loss of nuptial color in threespine sticklebacks (Gasterosteus aculeatus). Evolution 43, 450–60.

B. H. Seghers (1974). Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia 14, 93–8.

S. C. Stearns (1989). Trade-offs in life-history evolution. Functional Ecology 3, 259–68.

L. Szidat (1969). Structure, development, and behaviour of new strigeatoid metacercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada 26, 753–86.

T. Taugbøl , J. Skurdal & R. Andersen (1988). Ecological significance of differences in frequency of white fin margins among four brown trout (Salmo trutta) populations. Canadian Journal of Fisheries and Aquatic Sciences 45, 1304–9.

S. N. Thompson & M. Kavaliers (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109 (Suppl.), S119–S138.

J. F. Tierney , F. A. Huntingford & D. W. T. Crompton (1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 46, 603–5.

W. Wickler (1976). Evolution-oriented ethology, kin selection, and altruistic parasites. Zeitschrift für Tierpsychologie 42, 206–14.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 102 *
Loading metrics...

Abstract views

Total abstract views: 568 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 28th May 2017. This data will be updated every 24 hours.